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Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil Pseudomonas species.

ABSTRACT: High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple ¹³C-metabolomics experiments with Fe-replete and Fe-limited cells, we uncover how soil Pseudomonas species reprogram their metabolic pathways to prioritize siderophore biosynthesis. Across the three species investigated (Pseudomonas putida KT2440, Pseudomonas protegens Pf-5, and Pseudomonas putida S12), siderophore secretion is higher during growth on gluconeogenic substrates than during growth on glycolytic substrates. In response to Fe limitation, we capture decreased flux toward the tricarboxylic acid (TCA) cycle during the metabolism of glycolytic substrates but, due to carbon recycling to the TCA cycle via enhanced anaplerosis, the metabolism of gluconeogenic substrates results in an increase in both siderophore secretion (up to threefold) and Fe extraction (up to sixfold) from soil minerals. During simultaneous feeding on the different substrate types, Fe deficiency triggers a hierarchy in substrate utilization, which is facilitated by changes in protein abundances for substrate uptake and initial catabolism. Rerouted metabolism further promotes favorable fluxes in the TCA cycle and the gluconeogenesis-anaplerosis nodes, despite decrease in several proteins in these pathways, to meet carbon and energy demands for siderophore precursors in accordance with increased proteins for siderophore biosynthesis. Hierarchical carbon metabolism thus serves as a critical survival strategy during the metal nutrient deficiency.

SUBMITTER: Mendonca CM

PROVIDER: S-EPMC7768705 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil Pseudomonas species.

Mendonca Caroll M CM Yoshitake Sho S Wei Hua H Werner Anne A Sasnow Samantha S SS Thannhauser Theodore W TW Aristilde Ludmilla L

Proceedings of the National Academy of Sciences of the United States of America 20201203 51

High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple 13C-metabolomics experiments with Fe-replete ...[more]

PMID: 33273114

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Project description:High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple 13C-metabolomics experiments with Fe-replete and Fe-limited cells, we uncover how soil Pseudomonas species reprogram their metabolic pathways to prioritize siderophore biosynthesis. Across the three species investigated (Pseudomonas putida KT2440, Pseudomonas protegens Pf-5, and Pseudomonas putida S12), siderophore secretion is higher during growth on gluconeogenic substrates than during growth on glycolytic substrates. In response to Fe limitation, we capture decreased flux toward the tricarboxylic acid (TCA) cycle during the metabolism of glycolytic substrates but, due to carbon recycling to the TCA cycle via enhanced anaplerosis, the metabolism of gluconeogenic substrates results in an increase in both siderophore secretion (up to threefold) and Fe extraction (up to sixfold) from soil minerals. During simultaneous feeding on the different substrate types, Fe deficiency triggers a hierarchy in substrate utilization, which is facilitated by changes in protein abundances for substrate uptake and initial catabolism. Rerouted metabolism further promotes favorable fluxes in the TCA cycle and the gluconeogenesis-anaplerosis nodes, despite decrease in several proteins in these pathways, to meet carbon and energy demands for siderophore precursors in accordance with increased proteins for siderophore biosynthesis. Hierarchical carbon metabolism thus serves as a critical survival strategy during the metal nutrient deficiency. Data availability:The proteomics data have been deposited into the ProteomeXchange Consortium via the PRIDE partner repository with the data set identifier <a href='https://www.ebi.ac.uk/pride/archive/projects/PXD013605' rel='noopener noreferrer' target='_blank'>PXD013605</a>.

Project description:Iron (Fe) deficiency and toxicity are the most widely prevalent soil-related micronutrient disorders in rice (Oryza sativa L.). Progress in rice cultivars with improved tolerance has been hampered by a poor understanding of Fe availability in the soil, the transportation mechanism, and associated genetic factors for the tolerance of Fe toxicity soil (FTS) or Fe deficiency soil (FDS) conditions. In the past, through conventional breeding approaches, rice varieties were developed especially suitable for low- and high-pH soils, which indirectly helped the varieties to tolerate FTS and FDS conditions. Rice-Fe interactions in the external environment of soil, internal homeostasis, and transportation have been studied extensively in the past few decades. However, the molecular and physiological mechanisms of Fe uptake and transport need to be characterized in response to the tolerance of morpho-physiological traits under Fe-toxic and -deficient soil conditions, and these traits need to be well integrated into breeding programs. A deeper understanding of the several factors that influence Fe absorption, uptake, and transport from soil to root and above-ground organs under FDS and FTS is needed to develop tolerant rice cultivars with improved grain yield. Therefore, the objective of this review paper is to congregate the different phenotypic screening methodologies for prospecting tolerant rice varieties and their responsible genetic traits, and Fe homeostasis related to all the known quantitative trait loci (QTLs), genes, and transporters, which could offer enormous information to rice breeders and biotechnologists to develop rice cultivars tolerant of Fe toxicity or deficiency. The mechanism of Fe regulation and transport from soil to grain needs to be understood in a systematic manner along with the cascade of metabolomics steps that are involved in the development of rice varieties tolerant of FTS and FDS. Therefore, the integration of breeding with advanced genome sequencing and omics technologies allows for the fine-tuning of tolerant genotypes on the basis of molecular genetics, and the further identification of novel genes and transporters that are related to Fe regulation from FTS and FDS conditions is incredibly important to achieve further success in this aspect.

Dataset Information

Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil Pseudomonas species.

Publications

Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil <i>Pseudomonas</i> species.

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